SEX
DETERMINATION
F.A.E.CREW
iTHUEN'S MONOGRAPHS ON
QP BIOLOGICAL SUBJECTS
251
C 86 :
METHUEN'S
MONOGRAPHS ON
BIOLOGICAL SUBJECTS
General Editor: Michael Abercrombie
SEX-DETERMINATION
Sex-
Determination
F. A. E. CREW, F.R.s.
Professor of Social Medicine and
formerly Professor of Animal Genetics
in the University of Edinburgh
LONDON: METHUEN & CO. LTD.
NEW YORK: JOHN WILEY & SONS, INC.
First Published January 26th 1933
Second Edition October gth 1946
Third Edition, Revised^ 1954
3-1
CATALOGUE NO. 4115/U
PRINTED IN GREAT BRITAIN
PREFACE
The purpose of this book is to present the saUent facts
relating to sex-determination and to guide the student
to further reading. It presupposes that the reader al-
ready has a fair knowledge of genetics and cytology; it
restricts itself to a consideration of the cytological and
genetical aspects of sex-determination and does not
consider the problems that cluster round the actual
development of the sexual characters, since such de-
velopment pertains not to sex-determination but rather
to sex-differentiation.
Those who wish to explore more fully the matters
touched upon in this book are advised to turn to
Advances in Genetics ^ edited by M. Demerec, four
volumes of which have been published so far in 1947-
195 1 by Academic Press Incorporated, New York, and to
The Evolution of Genetic Systems by C. D. Darlington,
published in 1946 by the Cambridge University Press.
Such as wish to proceed from a study of sex- determina-
tion to one of sex- differentiation can profitably refer to
F. H. A. Marshall's Physiology of Reproduction, third
edition, edited by A. S. Parkes and published in 1952
by Longmans, Green, London, or to Sex atid Internal
Secretions, edited by Edgar Allen and published in 1939
by Williams and Wilkins Company, Baltimore.
^^^^^^ F.A. E. C.
EDINBURGH
1953
CONTENTS
Ctt\P. PAGE
PREFACE V
1 . THE GENETIC THEORY OF SEX-DETERMINATION I
2. THE SEX-CHROMOSOMES AND SEX-DETERMINATION.
THE SEX-RATIO 9
3. SEX-LINKAGE. NON-DISJUNCTION. GYNANDRO-
MORPHISM 18
4. SEX-DETERMINATION IN HABROBRACON, SCIARA AND
LYMANTRIA DISPAR 3°
5. GENETIC INTERSEXUALITY IN DROSOPHILA, CER-
TAIN LEPIDOPTERA AND BIRDS 42
6. SEX-DETERMINATION IN FISH AND THE LOWER ALGAE.
SEX IN PARAMECIUM AND FUNGI. SEX-DETERMINA-
TION IN BRYOPHYTES. SEX IN THE HIGHER PLANTS 46
7. SPECULATIONS CONCERNING THE EVOLUTION OF THE
SEX-DETERMINING MECHANISM 5 1
BIBLIOGIL\PHY 55
GLOSSARY
62
AUTHOR INDEX 65
SUBJECT INDEX 67
72336
Vll
CHAPTER I
THE GENETIC THEORY OF
SEX-DETERMINATION
Sex (L. seco, to cut), the distinction between male and female, the
property by which an individual is male or female. Sexuality, the
quality of being distinguished by sex.
From the ver^^ beginning of human existence a difference
between the two contrasted types we know as male and
female respectively must have been recognized. Within
every individual the force of sexuality has operated to focus
thought upon matters sexual and to yield an intense aware-
ness of the sexually contrasted form. It can safely be assumed
that this observed difference in mankind and in the animals
man domesticated has at all times intrigued the human mind
and provoked speculation concerning its significance and
causation. Every individual displays the property of sexu-
ality and by his own experience knows of it. Speculation con-
cerning it has never been restricted to students of biology;
any man can claim to be his own authority.
The observations that required an explanation were but
few to begin with. Maleness and femaleness were attributes
which were exercised in the sexual relationship. The sexual
union of male and female resulted in reproduction, in the
production of offspring among whom males and females
appeared in more or less equal numbers. In this production
by a male and a female of males and females there was to be
observed an orderliness and a precision which suggested that
some relatively simple mechanism was involved.
Hypotheses concerning the way in which and the time
during the life history of the individual at which sex is
determined have been plentiful. For the most part they
were elaborated at a time when little or nothing was known
of the anatomy and physiology of the cell, of cell division, of
gametogenesis and of fertilization, or they were constructed
by such as were unaware of, or chose to disregard, what was
I
2 SEX-DETERMINATION
known concerning these matters. Up to the beginning of the
present century each of them in its turn was destroyed when
it proved to be incapable of accommodating some new
observation. In retrospect it is easy to understand how it
came about that a theory derived from and based upon the
experience of an obstetrician, for example, could not be
stretched to include the outcome of the experience of a
breeder of habitually polytocous livestock.
Then, as the studies of the zoologist and of the botanist
widened to include an ever-expanding number of species, it
is understandable how it happened that a theory elaborated
by a zoologist proved to be of no value whatsoever to a
botanist who had encountered in his material phenomena
strongly resembling those of sexuality in the animal. That
for which men continually sought was a theory that could
accommodate all that was known about the phenomenon of
sexuality wherever it appeared, and as this knowledge ex-
panded the difficulties of constructing a satisfactory theory
of the causation of sex multiplied.
Each of these theories of sex-determination has to be
examined against the background of the total biological
knowledge that was in man's possession at the time when
the theory was promulgated. If it accommodated all the
observations thus far made, and if it was a reasonable,
intelligent groping after understanding, then in its day it was
a good and useful theory. That it is now unwarrantable in
the light of our vastly increased knowledge of matters
biological in no way robs the theory of its merit.
By the beginning of this century our knowledge of the
cell, of gametogenesis and of fertilization had become
greatly expanded, and in the earliest years of the century,
as an outcome of the confirmation of the Mendelian theory
of organic inheritance, much attention became focused upon
the mode of transmission of inherited characters and the
search began for the actual mechanism of segregation that
was postulated by the Mendelian theory. Thus it was that
the sciences of genetics and of cytology entered into a phase
of intensely active development.
The facts to be accommodated by a theory of sex-
GENETIC THEORY 3
determination could now be stated more exactly. In a wide
variety of species sex-dimorphism occurs; within them there
are males and females. Sexual reproduction, taking the form
of the fusion, permanently or temporarily, of two complete
individuals or parts thereof or in the union of single cells
derived from one and the same individual or from two
individuals, occurs in all those groups of organisms in
which the presence of a nucleus has been demonstrated.
In the higher forms sexual reproduction consists in the
formation of single cells, the gametes, the separation of
these from the rest of the individual and their subsequent
fusion in pairs to form the zygotes, the new individuals of
a new generation. In most of these forms two kinds of
gametes are to be found — a small, active, motile gamete
elaborated by the male (or by the testis of the herma-
phrodite) and a relatively large, inactive, non-motile gamete
elaborated by the female (or by the ovary of the herma-
phrodite). These gametes constitute the only organic bridge
connecting the generations.
Usually during spermatogenesis the nucleus and the
cytoplasm of a cell are equally divided among four functional
spermatozoa, whilst during oogenesis three of the products
of division are suppressed and extruded to become the polar
bodies, only one remaining to become the functional ovum.
The simplest form of spermatozoon consists of four parts:
(i) the nucleus forming the head; (2) the centrosome, a non-
nuclear body forming the middle piece from which the
axial filament of the vibratile tail is developed; (3) the mito-
chondria, bodies of non-nuclear origin which form the
sheath of this filament, and (4) ordinary cytoplasm which
forms a thin coat over the head and tail. The nucleus alone
is the constant constituent of the spermatozoon; it alone
fuses with the nucleus of the ovum. No other organ save
the centrosome takes any part in the development of the
new individual.
The essential feature of sexuality is the production of two
different kinds of gametes by the individuals of a species,
male-type by the male, female-type by the female. Fusion
between gametes is restricted to such as possess and display
4 SEX-DETERMINATION
contrasted characters (details of structure and of behaviour)
and usually to such as are derived from two sexuallv con-
trasted individuals.
The division of a cell into two by simple fission is no mere
casual cleavage; it is a process of precision, karyokinesis or
mitosis, the essential feature of which is the exact halving
of the two chief constituents of the cell, the nucleus and the
cytoplasm, so that the two daughter cells that result are
save in respect of initial size, exact copies of the cell that
produced them.
The most striking features of mitosis are the exact and
precise division of the chromosomes and the precise distri-
bution of the daughter chromosomes so formed. In respect
of their chromosome constitution the daughter cells are
exact copies of the mother cell that produced them.
In each and every species there is a characteristic number
ot chromosomes within the nuclei of its component cells
I;^or example, man has forty-eight (Evans and Swezy, 1020).
These exist in the form of pairs, the members of any given
pair (with one exception later to be considered) being alike
m size, shape and behaviour during cell-division.
This constancy of the chromosome number could not
exist if at fertilization both the egg and the sperm brought
into the new zygote that number of chromosomes which is
characteristic of the species. Offspring have the same num-
ber as the parents (polymitotic forms and polyploidy being
disregarded). Constancy is maintained by a reduction of the
chromosome number to a half during gametogenesis. The
existence of this process was postulated by Weismann
u ''Vxr, ^^ hypothesis has been verified universally since
then. Wherever there is fertilization there is also reduction
which in essence consists of two divisions of the nucleus of
the cell associated with one division of its chromosomes
with the result that four daughter nuclei are produced, each
ot these having half the number (the haploid number) of
chromosomes characteristic of the species. Meiosis, this
process of reduction, is a modification of mitosis.
Fertilization consists essentially in the bringing together
ot two half-sets of chromosomes and the consequent re-
GENETIC THEORY 5
establishment of the characteristic chromosome number.
One member of each of the pairs of chromosomes with
which the new individual is endowed comes by way of the
spermatozoon from the father; its mate comes by way of
the ovum from the mother.
Many of the details of structure and function that are
exhibited by the individual are the expression of the heredi-
tary constitution of the individual. Mendel postulated that
such characters were brought into being by the action of
'hereditary factors'. In every individual's constitution, and
in respect of any given character, there were two such factors,
only one of which passed into each gamete. Commonly, of
the pair of hereditary factors one was dominant, the other
recessive, the dominant one alone exerting an influence dur-
ing development. Thus an individual exhibiting the dom-
inant member of a contrasted pair of hereditary characters
could be either a homozygous dominant (DD) or else a
heterozygous dominant (Dd).
Mendel (1865) himself hazarded the suggestion that sex-
determination might prove to be a phenomenon of heredity
and segregation. Experimental evidence of its validity was
furnished as early as 1907 by Correns, who studied hybrids
between monoecious and dioecious species of Bryonia. His
results indicated that in the dioecious species sex was deter-
mined by the pollen grain of which there were two kinds
equal in number, one being male-producing and the other
female-producing whilst the ovules were all of a kind.
Correns compared the combinations resulting from the
union of the two forms of pollen grain with the one form of
ovule with those of the typical back-cross of a Mendelian
experiment in which the heterozygous dominant (Dd)
mated to a recessive (dd) yields equal numbers of hetero-
zygous dominants and recessives.
Dd X
dd
D
d :
d gametes
)d
I
dd
Doncaster (1906), working with the currant moth Abraxas
grossulariata, produced evidence that strongly suggested
6 SEX-DETERMINATION
that in animals also sex- determination was due to segrega-
tion of hereditary factors.
Bateson and Punnett (1908), basing their interpretation
on the assumption that the character femaleness was
dominant to the contrasted character maleness, and that the
female in Abraxas was always heterozygous in respect of
the character femaleness, devised a scheme, of considerable
historical interest, to show the relationship of the sex of the
individual to its colour pattern. If the hereditary factor for
the grossulariata colour pattern is symbolized by G, that for
lactocolor by g, that for the dominant femaleness character
by F, and that for the recessive maleness character by f, then
the results of Doncaster's experiments can easily be accom-
modated, if it is assumed that the female is always con-
stitutionally heterozygous (Ff) for the character femaleness,
and further, that the two dominant factors G and F repel
each other so that they can never be present together in the
same gamete.
The results of the breeding experiments carried out by
Doncaster were as follows:
1. lacticolor $ x gross. (^=gross. sons and daughters. Gross, was
dominant to lacticolor.
In the F.2 both gross, and lact. occurred, there being on the
average in every 4, 3 gross, to i lact. Among the gross, indi-
viduals there were both males and females but the lacticolors
were all females.
2. F.I gross. (^ X lact. $=gross. and lact. individuals in equal
numbers and among both of these types males and females in
equal numbers.
3. lact. S from 2 x F.i gross. $=equal numbers of gross, and lact.
individuals but all the gross, were males and all the lact. were
females.
4. lact. o from 2 x wild gross. $ = equal numbers of gross, and lact.
individuals but all gross, were males and all lact, were females.
Bateson and Punnett's explanation of these results was
as follows :
1. lact. $ X gross. <?
ggFf GGff P.I
gF gf : Gf gametes
GgFf Ggff F.I
gross. ? gross. <S
2.
GENE!
:ic
THEORY
7
Gf gF (repulsion)
J
Gf gf
gametes
GGfT Ggff
gross. (^ gross. 3
GgFf ggFf
gross. ? lact. ?
F.2
lact. $
ggFf
X
F.I gross. (J
Ggff
gF gf
:
Gf gf
gametes
GgFf ggFf
gross. ? lact. ?
Ggff ggff
gross. S lact. ?
F.I gross, $
GgFf
X
lact. c?
ggff
Gf gF (repulsion)
:
gf
gametes
Ggff
gross, o
ggFf
lact. ?
wild gross. $
GgFf
X
lact. (^
ggff
Gf gF (repulsion)
:
gf
gametes
Ggff
gross. (^
ggFf
lact. ?
Since the time when this explanation of what is now
known to be an instance of the inheritance of sex-linked
characters was offered, the sciences of cytology and genetics
have expanded vastly and out of their development emerged
the current theory of sex-determination. By this theory all
the older hypotheses of sex-determination have been ren-
dered obsolete and, save for historical purposes, can be
disregarded. The framework of this theory consists of secure
knowledge concerning the constant and significant differ-
ences between male and female in respect of their sex-
chromosome and therefore of their genie constitution and,
secondly, concerning the observed facts relating to the
phenomenon of sex-linkage, which enables the observer to-
trace the transmission of sex-chromosomes from generation
to generation. The primary difference between the sexes is
now known to be a chromosomal and a genie difference. In
the bisexual and dioecious species the sex of the individual,
as a general rule, is now known to be decided at the moment
of fertilization by the interplay of the sex-chromosome
constitutions of the uniting gametes. This chromosomal,.
8 SEX-DETERMINATION
genetic, theory was confirmed by the correlation that has
been observed between the distribution in inheritance of the
sex-chromosomes and of the sex-Hnked characters. Nothing
that has been encountered during the last fifty years has
required any significant modification of this theory. At
present it seems distinctly unlikely that this theory will be
at all seriously shaken in foreseeable time, but new dis-
covery in other scientific fields may, in its impact upon
biological science, necessitate its review and revision.
CHAPTER 2
THE SEX-CHROMOSOMES AND
SEX-DETERMINATION
In a very large number and in a wide variety of species it has
been shown that the male is to be distinguished from the
female by constant differences in the chromosome content
of the nuclei of their component cells. This difference takes
several forms. In certain species one sex possesses one
chromosome less than does the other, that is to say in one
sex the chromosomes are all paired whilst in the other one
member of one pair is lacking. In other species both sexes
possess the same number of chromosomes, existing in pairs,
but in one sex one particular pair consists of chromosomes
unequal in size and shape.
The single unpaired chromosome found in one sex and
the pair in the other to which it corresponds, and the pair of
chromosomes in respect of which the sexes differ, are known
as the sex-chromosomes in order to distinguish them from
the rest of the chromosomes in respect of which both male
and female are alike. These are known as the autosomes.
The single chromosome found in one sex and the pair in the
other to which it corresponds and, in the case of the species
in which the chromosome number is the same in both sexes,
that chromosome which is found in both male and female,
are known as X- chromosomes. The unequal mate of the X
in one of the sexes is known as the Y-chromosome. Thus m
respect of sex-chromosome constitution the sexes can be
described as:
XO:XX
or XY:XX
The third form which this difference between the sexes
takes is that in which the sex-chromosomes are represented
not by single elements but by groups which during gameto-
genesis behave as one compound chromosome. Whatever
2 9
10 SEX-DETERMINATION
the number of X-chromosomes within the group, the group
itself is single in one sex, double in the other, so that
essentially this difference is of the XOrXX type or, as is
sometimes the case, XY:XX, for the single compound X is
in certain species associated with a Y-chromosome. Ray-
Chaudhuri and Manna (1950) report that the male of the
gryllid Euscyrtus is X^X^Y. The Y can itself be compound.
Thus in the dioecious plant Rumex acetosa Kihara and Ono
(1923) found a Y-chromosome consisting of two elements
in association with a single X. According to Sharman,
Mcintosh and Barber (1950) the rat kangaroo is XY^Y^ in
the male, XX in the female.
The first account of a sex-chromosome difference was that
of Henking (1891), who described in the bug Pyrrhocoris
apterus a peculiar chromatin element which was condensed
in the early prophase of the primary spermatocyte. In the
first spermatocyte division the twelve elements found in the
metaphase plate all divided equally, but in the second divi-
sion one of the twelve elements lagged and finally passed
undivided into one of the two daughter cells. As a result two
kinds of spermatids were formed, one with eleven and one
with twelve of these elements. Henking did not at this time
refer to this odd chromatin element as a chromosome but
called it a 'nucleolus'. He did not confuse it with a true
nucleolus, however.
In 1898 Paulmier recorded a similar phenomenon in
Anasa tristis, in the second spermatocyte division of which
eleven chromosomes passed to one pole and ten to the other.
In 1 90 1 de Sinety described the behaviour of what he called
a 'chromosome special' in the male of Orphania. In the
same year McClung suggested that the two classes of
spermatozoa resulting from the meiotic distribution of the
'accessory' chromosome must be causally related to the
production of the two sexes. 'Upon the assumption that
there is a qualitative difference between the various chromo-
somes of the nucleus it would necessarily follow that there
are formed two kinds of spermatozoa which, by fertilization
of the egg, would produce individuals qualitatively different.
Since the number of each of these varieties of spermatozoa
SEX-CHROMOSOMES II
is the same, it would happen that there would be an approxi-
mately equal number of these two kinds of offspring. We
know that the only quality which separates the members of
the species into these two groups is that of sex.'
Thus it was that the chromosome complex came to be
associated with sex-determination. McClung's main hypo-
thesis was complicated by its association with a subsidiary
one of selective fertilization which led him to the conclusion
that the spermatozoon carrying the extra chromosome was
male-determining. If this were so, then the male had to be
the sex which had one chromosome more than did the
female. Sutton (1902), by reporting that the spermatogonia
of Brachystola possessed one chromosome more than did
the ovarian follicle cells, provided support for McClung's
error.
The work of McClung aroused great interest and much
controversy. It evoked great activity in the field of cytology.
Gross (1906) claimed to have demonstrated that in Syro-
mastes and Pyrrhocoris the accessory chromosome (the
single, unpaired one) present in the spermatocytes arose
from two small spermatogonial chromosomes and, further,
that the number of chromosomes was the same for both
sexes. It was his opinion that all spermatozoa lacking the
accessory chromosome degenerated so that only one type of
functional gamete remained. However, Stevens (1905) m the
beetle Tenebrio and Wilson (1905) in the bug Lygaeiis
furcicus showed clearly that in these forms at least there was
one pair of unequal chromosomes and that this pair behaved
in the growth stages of the spermatocytes exactly like the
unpaired accessory chromosome. They found also that the
members of this unequal pair separated and passed to oppo-
site poles in one of the two meiotic divisions. Stevens further
demonstrated that the diploid number of chromosomes was
the same in both sexes but that in the female no pair con-
sisting of unequal mates was present, the male being XY,
the female XX. Then in 1909 Wilson corrected Gross by
showing that in the male of Pyrrhocoris there was an un-
paired chromosome in the spermatocyte and that this arose
from a single spermatogonial chromosome of corresponding
12 SEX-DETERMINATION
size and not, as Gross thought, from a pair of smaller
spermatogonia! chromosomes. In the case of Syromastes
Wilson showed that Gross was correct in his observation
that these two chromosomes represented the components
of a compound sex-chromosome which was unpaired. In the
female each of the two components was represented twice so
that the diploid number was greater by two chromosomes
than was that of the male.
It thus appeared that the X-chromosome was the sex-
determining agent, one X yielding a male, two XX's a
female, the Y-chromosome itself exerting no discernible
influence. This heterogamety on the part of the male and
this homogamety on the part of the female were responsible
for the production of a sex-ratio of equality in the next
generation.
Male Female
X-
XX
X - :
XX
X
X-
gametes (two forms of spermatozoa,
one form of ova)
fertilization
Females Males
in equal numbers
The XO=male; XX=female type of sex-determining
mechanism is commonly known as the 'Protenor type'. In
this form the male is the heterogametic sex. Half of the
spermatozoa produced by the male contain one X-chromo-
some and are female-producing, while the other half lack
such a chromosome and are male-producing. The diploid
chromosome number in the female is a multiple of two; the
chromosome number in the male is one less. In Protenor
belfragi the diploid number in the female is 14, whilst in the
male it is 13. Since in this species the X-chromosome is at
least twice the size of any of the autosomes it is readily
recognized. The single X-chromosome of the male is always
derived by way of the egg from the mother, passes from the
male to the female in the production of females and from
the female to the male in the production of males.
The fact that in maturation each ovum received a single
SEX-CHROMOSOMES I3
X-chromosome was first established through the work of
Morrill (1910) on the maturation of the egg in various
hemiptera, of Boveri (1909) and Gulick (191 1) on the
nematode Heterakis and of Mulsow (1912) on the nematode
Ancyracanthus cystidicola. In the last of these forms the
chromosomes remain separate in the spermatozoon so that
they can be counted. The primordial egg cells in the ovary
contain 12 chromosomes. During synapsis 6 double ele-
ments are to be seen. The first maturation division removes
6 complete chromosomes from the egg into the polar
body; the second maturation division splits each remain-
ing chromosome longitudinally and separates the resulting
halves. The mature tgg therefore comes to possess 6 chromo-
somes, one of these being the X.
In the case of the male gamete the primordial germ cells
of the testis include only 1 1 chromosomes, one of which is
the unpaired X. When these chromosomes conjugate in the
synapsis stage the X-chromosome has no partner and it
remains apart from the others in the resting nucleus. In the
first maturation division there are 5 bivalent chromosomes
and the univalent X. When the chromosomes are distri-
buted to the daughter cells the X passes undivided to one
of these. This heterotypic division yields two primary
spermatocytes, one with 5 chromosomes, the other 6. The
homotypic division cleaves each of these primary spermato-
cytes into two by ordinary mitosis with the result that four
spermatids are formed, two of them with 5 and two with
6 chromosomes. During their maturation into spermatozoa
the chromosomes remain visible and it is possible to observe
that the eggs are fertilized by 5 chromosomes and 6 chromo-
somes bearing spermatozoa respectively.
Later cytological work showed that the Protenor type is to
be found in most orthopterans, many bugs, beetles, spiders,
myriapods and nematodes. Hughes- Schrader (1947), for
example, lists 17 species of the bisexual Phasmids which are
XO in the male.
The Lygaeus type is commonly regarded as a more
primitive form from which the Protenor type was derived
through the progressive loss of the Y-chromosome. It is
14 SEX-DETERMINATION
characterized by the presence of a synaptic mate for the X.
The diploid number of chromosomes is the same in both
sexes.
Male Female
XY X XX
X Y : X gametes
XX : XY fertilization
Females Males
in equal numbers
All the mature ova of the female receive a single X. The
Y is strictly confined to the male line. The son receives his
Y from his father and his X from his mother. The daughter
receives one X from each of her parents.
The Y commonly, though by no means invariably, is
smaller than the X. In the majority of instances the X and
the Y are disjoined in the first or heterotypic division, each
dividing equationally in the homotypic division. During the
growth period of the spermatocytes both the X and the Y
typically undergo heteropycnosis and in most instances they
unite to form a single bivalent. This then separates into its
two components so that half the sperm receive an X, the
other half a Y.
The XY pair differs from the autosomes in that they
usually do not take part in the synaptotene stages or in the
formation of tetrads. There is a tendency for the X and the
Y to come together during prophase. In many instances their
contact is but slight so that the two chromosomes can still
be distinguished. In other cases the union which occurs
during the growth stages of the meiotic period is a much
more intimate one and the two chromosomes are contained
within a single chromosome nucleolus. The joined X and Y
may enter into the primary spermatocyte spindle in the form
of a tetrad. But the inequality of the X and Y can usually
be recognized in these structures and therefore the presence
of a tetrad does not necessarily indicate any actual synapsis.
The Lygaeus type of sex-chromosome sex-determining
mechanism is to be encountered in mammals and dioecious
plants, is common in diptera and not unusual in bugs and
beetles. The size difference between the X and the Y varies
SEX-CHROMOSOMES 15
greatly from species to species; the Y may be exceedingly
small or it can be equal in size to the X. Among the bugs
there are species which can be graded according to the
relative size of the Y, from those in which the Y is as large
as the X to those in which the Y is absent.
Hetero- or di-gamety is not a property of the male, how-
ever. In birds and lepidoptera it is the female that is hetero-
gametic and the male that is homogametic.
The male of the domestic fowl has an even number of
matched chromosomes, including seven pairs of large ones
and fifteen pairs of small ones. Sokolow, Tiniakow and
Trofimov (1936) concluded that the sex-chromosome was
a V-shaped chromosome with arms of equal length which
was present in duplicate in the male and in the simplex state
in the female. They found it impossible to decide whether
or not one or other of the many small chromosomes was the
Y in the female. Pheasants, peafowl and turkeys were found
to have the same kind of sex-chromosome constitution. In
the guinea-fowl and woodcock there were two such chromo-
somes in the female, four in the male.
Among the lepidoptera Seller (1920) found in the moth
Talaeporia tuhidosa 60 matched chromosomes in the male
and 59 in the female which synapsed into 29 pairs and an
unpaired univalent.
The difference between male and female heterogamety in
no way affects the functioning of the mechanism.
Male
Female
XX
X XO or XY
X
: X
orX
0 gametes
Y
XX
: XO
orXY
fertilization
Males Females
The compound sex-chromosome mechanism has been
encountered in Tenodera, Paratenodera, Mantis, Stag-
momantis and in Hierodula, the males being X^XaY and the
females X1X1X2X2 (Oguma, 1921; King, 1931; Asana, 1934).
More recent work (White, 1938, 1941; Hughes- Schrader,
l6 SEX-DETERMINATION
I943» 1948, 1950; Matthey, 1949; Oguma, 1946) has shown
that not all the Praying Mantis have this type of sex-
chromosome mechanism, the males of many genera being
XO. It has been suggested (White, 1941; Hughes- Schrader,
1950) that the compound type arose from the more primi-
tive XO type through a structural rearrangement or series
of rearrangements. Possibly a single mutual translocation
between a metacentric X and a metacentric autosome con-
verted the original XO mechanism into the X^XgY mechan-
ism without any intermediate steps. If this is so, then the Y
is the homologue of the autosome involved in the trans-
location. In the grasshopper Paratylotropidia hrunneri King
and Beams (1938) found the sex-chromosome mechanism
likewise to be XiX2Y=male, XiXiX2X2= female.
The Sex-Ratio. The homo- heterogametic mechanism
described above should yield a sex-ratio among the newly
conceived, a primary sex-ratio, of equality. This numerical
relationship of males and females is expressed either as so
many males per 100 or per 1,000 females within the group
or else as the percentage of males among all the newly
conceived. It is impossible to determine the primary sex-
ratio among such forms as fishes, birds and mammals by
direct observation. It is necessary to examine a sufficient
number of foetuses and embryos as near to the point in
their development at which the differences that distinguish
the sexes can be recognized. When this is done it is found
that the sex-ratio among them is not one of equality though
not far removed therefrom. This 'foetal' sex-ratio ranges
from 44-5 per cent, males in some of these studies to 56-8 in
others. {Handbook of Biological Data.)
These observations do not destroy the validity of the
argument concerning the homo- heterogametic mechanism.
They are to be explained in different instances by one or
other of the following phenomena:
1. The two forms of gametes elaborated by the hetero-
gametic sex are not always produced in equal numbers.
2. These two forms are not invariably equally efficient
fertilization.
SEX-CHROMOSOMES 17
The two forms of zygote resulting from fertilization
are not always equally viable so that almost from the
beginning a sexually selective mortality operates to
produce a sex-ratio of inequality among the products
of conception and therefore among the newly-born
(the secondary sex-ratio).
CHAPTER 3
SEX-LINKAGE. NON-DISJUNCTION
GYNANDROMORPHISM
Sex-Linkage. When describing the transmission of a char-
acter from parent to offspring it is not necessary in the great
majority of instances to make any reference to the sex of the
parent or of the offspring; it is enough to state that, for
example, the dominant character exhibited by one of the
parents is displayed by all or by 50 per cent, of the offspring,
or that the recessive character exhibited by one of the
grandparents reappears in approximately 25 per cent, of the
grandchildren. In certain instances, however, like that of the
grossulariata and lacticolor characters of Abraxas, a correct
description involves reference not only to the distribution
of these characters among the individuals of the different
generations but also to the sex of the individuals that display
these characters.
Although the exact chromosome constitution of Abraxas
is unknown, the results obtained by Doncaster can be most
easily explained as follows. Assume that Abraxas has the
Lygaeus type of sex-chromosome constitution, that the
female is the heterogametic sex, that the genes for the char-
acters grossulariata and lacticolor are resident in the
X-chromosome (in any one X there being either that for
grossulariata or else that for lacticolor), and that there are
no genes in the Y that in any way interfere with the action of
these X-borne genes.
I. lact. ?
(gX)Y
(gX) Y
(GX)(gX)
heterozygous
gross, c?
(GX) (gX)
gross. S
(GX)(GX)
(GX)
(GX)Y
gross. $
(GX) Y
P.I
gametes
F.I
gametes
18
SEX-LINKAGE
19
(GX)Y
gross. $
(gX)Y F.2
lact. ?
2.
heterozygous
gross. S
(GX)(gX)
(GX) (gX)
(GX)Y (gX)Y
gross. ^ lact. ?
lact. c?
(gX)(gX)
(gX)
(gX)Y
lact. ?
gametes
gametes
(GX)(GX) (GX)(gX)
homozygous heterozygous
gross, o gross, o
lact. ? :
(gX)Y
(gX) Y
(GX)(gX) (gX)(gX)
homozygous heterozygous
gross, o gross, o
3. F.I gross. ? "
(GX)Y
(GX) Y
(GX)(gX)
heterozygous
gross, o
4. As 3 above.
In the domestic fowl the phenomenon of sex-linkage —
this association in inheritance of a discernible character and
of the character of sex itself — has in recent years formed the
basis of a large industry. Day-old chicks, every one of them
guaranteed to be a female, are sold by the thousand every
year. The seller does not examine their genitalia in order to
determine whether the chick is a male or a female; its sex
is signalled by its plumage coloration. As an example the
plumage characters barred and non-barred may be cited.
A non-barred (black) cock mated with barred hens produces
barred male and non-barred female offspring. Sons 'take
after' their mother, daughters 'after' their father, a
phenomenon known as criss-cross inheritance.
The actual sex-chromosome constitution of the domestic
fowl is not yet finally established, the number of chromo-
somes is very large and many of them are very small.
Assume that it is of the Lygaeus type with female hetero-
gamety. Assume further that the genes for the characters
barred and non-barred are X-borne and that barred is
dominant. A non-barred cock must then have the constitu-
tion (bx)(bx) and the barred hen (BX)Y.
20
SEX-DETERMINATION
Non-barred ^
(bx)(bx)
(bx)
(BX)(bx)
heterozygous
barred (J
Barred ?
(BX)Y
(BX) Y
(bx)Y
non-barred
$
gametes
The day-old chick that will develop into a barred-
plumaged bird has a white spot on the top of the head*
those who will not be barred when adult lack this spot. The
barred birds are male and can be separated from the females
among day-old chicks.
The sons of this mating are barred because to be males
they must possess two X-chromosomes, and because one of
these must come from their barred mother who has only
one to offer, one carrying the dominant barred gene. The
daughters of this mating are non-barred because to be
femal^ they must receive their Y from their mother and
their X from their father who has only one kind of X to
offer, an X carrying the recessive gene for the non-barred
character.
If the reciprocal cross is made and a barred cock is mated
with non-barred hens all the F.i, males and females alike,
are barred. In the F.2 there appear on the average in every 4
3 barred and i non-barred. Among the barred there are two
males and one female in every three and all the non-barred
are females.
Barred (^
(BX)(BX)
(BX)
(BX)(bX)
heterozygous
Barred (^
(BX) (bX)
(BX)(BX) (BX)(bX)
homozygous heterozygous
Barred (^ Barred c?
Non-barred $
(bX)Y
(bX) Y
(BX)Y
Barred ?
P.I
gametes
F.I
(BX) Y gametes
(BX)Y (bX)Y F.2
Barred ? non-barred ?
The recessive character of the grandmother is exhibited
by none of her sons or daughters and only by 50 per cent.
SEX-LINKAGE 21
of her granddaughters. These facts can be explained most
readily on the assumptions that the genes for the characters
barred and non-barred are being distributed by a mechan-
ism that at the same time is distributing the elements of a
sex-determining mechanism and, secondly, that the male of
the domestic fowl has in his constitution the sex-determin-
ing element in duplicate whilst the female possesses it in the
single state and is heterogametic. Homo- and heterogamety
require that there shall be a qualitative or quantitative
difference of this kind between male and female.
In man there is a form of the disease haemophilia that
behaves in inheritance in exactly the same way and which
goes far to prove that the male is heterogametic and that
haemophilia is a sex-linked recessive character, its gene
being X-borne. Evans and Swezy (1929) offered cytological
proof that man has the Lygaeus type of sex-chromosome
constitution, the male being XY.
It will be noted that according to this explanation (on
p. 22) there can be two kinds of males, haemophiliacs and
normals, and three kinds of females, normals, carriers and
haemophiliacs. This is so because the male has but one X-
chromosome and the female two. On any one X there can
be either the gene for normality or else the gene for haemo-
philia. In the case of the female the haemophilia gene can
be present in neither, in one or in both of the X's. A male
cannot be a carrier. It is because the carrier female is so
difficult to identify that she constitutes a danger to her off-
spring by a normal male. A female can be haemophilic only
when her father is a haemophiliac and her mother either
a carrier or else a haemophiliac. Haemophilia is seldom
encountered in the human female for the reason, it would
appear, that female haemophiliacs die in utero.
Non-Disjunction. That the mechanism that is concerned
with the distribution of these sex-linked characters is at the
same time the mechanism which in its functioning is in-
volved in the determination of the sex of the individual was
proved beyond all doubt by the work of Bridges (19 16) on
non-disjunction in Drosophila melanogaster.
22
SEX- DETERMINATION
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NON-DISJUNCTION 23
The science of genetics owes more to the fortuitous selec-
tion by T. H. Morgan and his colleagues at Columbia
University in the early days of this century of Drosophila
melanogaster as an experimental material than to any other
event that has occurred during its development. It so hap-
pened that this small fly possessed every possible attribute
that the geneticist could wish to find. It thrives under
laboratory conditions, it multiplies rapidly and it con-
tinually threw up mutant forms at a time when the geneticist
was seeking new phenotypes to explore. When the chromo-
some complex came to be recognized as the mechanism
involved in the transmission of the hereditary char-
acters, it was found that in respect of chromosome
number Drosophila possessed but four pairs, easily dis-
tinguished one from the other and that the X and Y of the
male differed markedly, so that cytologically the fly was as
excellent a material as it had proved to be genetically. Then
when cytological inquiry came to overtop the purely
genetical in importance it was found that in the fly's salivary
glands the chromosomes existed in a giant form. To a very
large extent the choice of Drosophila at that time deter-
mined the rate and the direction of the development of
genetics thereafter; it also affected profoundly the develop-
ment of the whole range of the biological sciences to give to
the Theory of the Gene an importance not less than that of
Evolution Theory itself.
An early mutation in Drosophila was the recessive sex-
linked white-eye character. It was quickly explained as
indicated below:
Wild type X Mutant
red eyed o white eyed ?
(WX)Y (wX)(wX) P.I
(WX) Y : (wX) gametes
(WX)(wX) (wX)Y F.I
red-eyed white-eyed
daughters sons
But to this rule there were exceptions, a number of
white-eyed daughters and of red-eyed sons making their
24
SEX-DETERMINATION
appearance. Bridges showed that these exceptional indi-
viduals could be explained if it were assumed that the
white-eyed mother was not (wX)(wX) but (wX)(wX)Y
in respect of sex-chromosome constitution, if a definite
abnormality in the distribution of the sex-chromosomes had
occurred during the maturation of the egg from which she
sprang.
Normally, of the two X-chromosomes in the unripe egg^
one during the reduction division passes into the polar body.
If exceptionally these X's did not so disjoin, both remaining
in the egg, or if both passed into the polar body, then two
further kinds of mature ova would result, one with two X's,
each in this case carrying the gene for white-eye (wX), and
the other without any X. The spermatozoa of the red-eyed
male are of two kinds, one with an X carrying the dominant
red-eye gene, the other with a Y. Fertilization of these two
exceptional kinds of egg would then yield four combina-
tions, so:
Eggs abnormal in respect of
sex-chromosome constitution
Spermatozoa
(wX)(wX) X
(-) no X chromosome
(WX)
Y
Phenotype
Sex-chromosome
constitution
I.
(WX)(wX)(wX)
red-eyed female
triplo-X
2.
(wX)(wX)Y
white-eyed female
XXY
3-
(WX)(-)
red-eyed male
XO
4-
(-)Y
?
-Y
I.
z.
Exhibits poor viability.
An exceptional white-eyed female. She exhibits this charact
because she received both of her X's from her mother.
An exceptional red-eyed male. He received his X from his father
and not from his mother.
Does not appear.
The mating of a normal red-eyed male to a non-disjunc-
tional white-eyed female (2 above) will yield the following
results:
NON-DISJUNCTION
25
normal red-eyed 0
X non-disjunctional XXY
white-eyed $
(WX)Y
(wX)(wX)Y
(WX) Y
: (wX)
Four kinds of gametes,
(wX)Y
the numerical propor-
tions of these being de-
(vvX)(wX)
termined by the fre-
Y
quency of the different
groupings of the triad
components and by the
variation of their posi-
tions on the spindle.
Fertilization
Phenot>'pe
Sex-chromosome
constitution
I.
(WX)(wX)
red-eyed ?
normal XX
2.
(WX)(wX)Y
red-eyed ?
XXY
3-
(WX)(wX)(wX)
red-eyed ? ?
triplo-X
4-
(WX)Y
red-eyed ^
normal XY
5-
(wX)Y
white-eyed <^
normal XY
6.
(wX)YY
white-eyed (^
XYY
7.
(wX)(wX)Y
white-eyed $
XXY
8.
YY
— i
? YY
Classes 3, the trisomic red-eyed female, and 8, the double
Y lacking an X, do not appear. 4, the exceptional red-eyed
male, has its origin in an X from the father and a Y from the
mother. 7, the exceptional white-eyed female, derives both
X's from the mother. She is a female because she is XX.
The exceptional white-eyed females (7) when mated with
normal red-eyed males always yield the same kind of ex-
ceptional offspring; the exceptional red-eyed males (4)
always behave as normal red-eyed males, they have a per-
fectly normal sex-chromosome constitution even though the
X and the Y are derived from the wrong parents. There are
two kinds of white-eyed males (5 and 6), one perfectly
normal, the other cytologically exceptional and therefore
producing exceptional gametes in its turn. 6 should be able
to yield an XXY female by fertilizing an X-bearing egg. It
does. The XXY female has been identified both genetically
and cytologically. Sex-determination would therefore seem
to be an affair of the sex-chromosome combination, no
26
SEX-DETERMINATION
matter how this may be estabhshed. Since in these non-
disjunctional types the autosomes are the same in both
sexes, maleness and femaleness would seem to be characters
that are based upon the number of X-chromosomes present
in the zygote. It would appear from this work of Bridges
that the X-chromosome itself is neither male-determining
nor female-determining but is of such a kind that when one
is present in association with a diploid set of autosomes
development is swung in the direction of maleness, whereas
when two are present it is swung in the direction of female-
ness. The egg possesses the capacity to develop in either
direction, the direction taken being determined by the rela-
tive amount of X-chromosome-borne chromatin.
Then in 1922 came the work of L. V. Morgan on attached
X-chromosomes which finally showed that two X's in the
zygote, irrespective of their origin, resulted in the produc-
tion of a female. The culture of Drosophila used by L. V.
Morgan exhibited a sex-linked recessive character yellow
body-color. Homozygous yellow females mated to wild-
type (grey body-colored) males gave only yellow daughters
and grey sons, a constant and complete reversal of the ex-
pected criss-cross mode of inheritance. Cytological examina-
tion showed that in these females instead of the usual two
X's there was a single V-shaped chromosome and, in
addition, usually a supernumerary Y. Others possessed a
single X in addition to this V. The V was shown to be two
attached X's which did not disjoin during meiosis.
An attached X
Normal
Yellow $
Greyed
(gX)-(gX)Y
X (GX)Y
(gX)-(gX)
Y
(^^) jgametes
Phenotype Sex-chromosome
constitution
(i) (gX)-(gX)(GX)
grey female triplo-X
(2) (gX)-(gX)Y
yellow female XXY
(3) (GX)Y
grey male XY
(4) YY
? YY
G=the gene for grey body-colour; g=yellow; ^=attached.
(i) rarely survives. (4) is non- viable and does not appear.
GYNANDROMORPHISM 27
Thus the addition of a Y to XX has no discernible effect
upon the sex-differentiation of the individual. The X-bear-
ing sperm which usually takes part in the creation of a
female here contributes to the origin of a male if it fertilizes
a Y-bearing egg. Sex is thus determined by the sex-
chromosome distributing mechanism which operates at the
time of karyogamy.
It is now established that the Y-chromosome is not com-
pletely inert. Part of it is inert but there is a portion which
carries genes and which is homologous gene by gene with
the X-chromosome. Both Bridges and Stern (1927) have
identified 'fertility' genes in the Y and Sturtevant showed
that the reason why the males of a 'bobbed' stock do not
exhibit this recessive sex-linked character is that there is a
dominant normal gene in the Y.
Gynandromorphism. The essential feature of the con-
dition of gynandromorphism is the presence in one and the
same individual of a species in which sex-dimorphism is the
rule, of sharply defined regions of the body some of which
show the characters of the male, others of which display the
characters typical of the female. A gynandromorph is a sex-
mosaic in space. A 'lateral' gynandromorph has one half of
the body, the left or the right, including the reproductive
organs, completely male in its characterization while the
other half displays the typical female characterization; in an
anterior-posterior gynandromorph the anterior half of the
body has the characterization of one of the sexes, the
posterior half those of the opposite sex. The sex-mosaic can
be much less regular than this, however, most of the
regions of the body displaying the characters of one
sex and only a relatively small area exhibiting those of the
other.
Time came when this phenomenon of gynandromorphism
could with great advantage be investigated in Drosophila
melanogaster . The genetic and cytological analysis of this
fly came to be very advanced. The spacial relationships in
the different chromosomes, both autosomes and sex-chro-
mosomes, of several hundreds of genes were quickly
28 SEX-DETERMINATION
determined by planned experimentation. Gynandromorph-
ism is not uncommonly encountered in this form.
Morgan and Bridges (1919) showed that in these Droso-
phila melanogaster gynandromorphs whereas the trans-
mission of the autosomal characters was not affected, both
male and female parts displaying them equally, that of the
characters the genes for which were X-chromosome-borne
was disturbed. It was possible therefore to conclude that in
such a gynandromorph the male and female regions differed
from each other in respect of the X-chromosome content of
the nuclei of their component cells.
A lateral gynandromorph with a white-eyed side display-
ing the male characterization and a red-eyed side exhibiting
the female characterization can be explained as follows:
White eyed ^ x Red eyed $ Parents
(wX)Y (WX)(WX)
(WX)(wX) the gynandromorph in its
beginning
The gynandromorph started its life as an XX individual,
being the result of the fertilization of an t^g with an
X-chromosome carrying the dominant gene for red-eye by
a spermatazoon with an X-chromosome carrying the reces-
sive gene for the white-eye character. At the first division of
this fertilized tgg when each of these X's splits longi-
tudinally and when normally each of the nuclei of the two
resulting daughter cells receives two daughter X's, one
paternal and one maternal in origin, one of these daughter
X's — the maternal one carrying the dominant red-eye gene
— became excluded from one of the daughter nuclei. The
sex-chromosome constitution of the two daughter nuclei
therefore came to be:
(wX) : (WX)(wX)
Then if from each of these cells there arose the tissues of one
lateral half of the body and if the single X constitution
equals maleness and the XX constitution leads to the
development of femaleness, a *half sider' should result, one
side being male and white-eyed, the other female and red-
eyed.
GYNANDROMORPHISM 29
If this explanation is valid, then gynandromorphism in
Drosophila melanogaster is the result of the elimination of an
X-chromosome from the nucleus of one of the cells pro-
duced by the first cleavage division of a female zygote (XX).
XO tissue is male tissue. If such elimination occurs at the
second cleavage division a quarter of the body becomes XO
in constitution and male in characterization. The later in
embryonic development this elimination occurs the less will
be the amount of male tissue in such an individual. When
in an elimination gynandromorph the abdomen is affected
and is male-type, the individual behaves as a male but is
invariably sterile.
Morgan and Bridges (19 19) found in a series of about a
hundred that the maternal X was eliminated about as
frequently as was the paternal.
Doncaster (1914) noted that in the moth Abraxas there
was occasionally to be encountered an egg with two separate
maturation spindles and two female pronuclei each about to
be fertilized by a separate sperm. If each of these pronuclei
was fertilized by a separate spermatozoon, and if one of these
was X-chromosome-bearing, the other Y-chromosome-
bearing, such double fertilization could yield a gynandro-
morph. Bridges (Morgan, Bridges and Sturtevant, 1925)
came across such a dizygotic gynandromorph in Drosophila
melanogaster in a back cross involving the recessive char-
acters speck and vestigial, the genes for which are resident
in the second chromosome. The right side of the body was
predominantly female and displayed the character speck;
the left side was mostly male and exhibited the vestigial
wing character. The ovum had two nuclei, in each of which
was an X and a 2nd chromosome. One of these nuclei united
with a sperm carrying an X and a 2nd, the other with a
sperm with a Y and a 2nd. From each of these fertilized
nuclei one side of the body developed.
Egg nucleus Sperm
Right side X 2nd speck X 2nd vestigial speck
Left side X vestigial Y vestigial speck
Only rarely was it found that these dizygotic mosaics differed
laterally in respect of the sex-characters.
CHAPTER 4
SEX-DETERMINATION IN HABROBRACON,
SCIARA AND LYMANTRIA DISPAR
Habrobracon. As long ago as 1845 Dzierzon observed that
in the honey-bee the sex of the individual was determined
by the occurrence or non-occurrence of fertilization; the
egg being fertilized gave rise to a female; the egg not being
fertilized and developing parthenogenetically yielded a male.
This difference was later interpreted as a difference between
diploidy (in respect of the chromosomes) and haploidy and
was found to be characteristic of the hymenoptera generally.
The possible evolutionary origin of this haplo-diploid sex
determining mechanism has been reviewed by White (1945)
and Whiting (1945).
When Bridges formulated his concept of genie balance it
became necessary to discover whether or not the facts relat-
ing to parthenogenesis could be newly interpreted. Accord-
ing to this concept the haploid stated yielded maleness as
did also this state in duplicate. If diploidy was to yield
femaleness, then the two sets of chromosomes had to
be qualitatively different so that where iN=maleness,
N+N'=femaleness.
That this is so has been shown by Whiting and his school
working with the wasp Habrobracon juglandis which is
parasitic on larvae of the meal moth Ephestia. Torvik-Greb
(1935) showed that in Habrobracon the female is diploid
with 20 chromosomes and the male haploid with 10. The
reduced egg has a set of 10 and the sperm, through an
aborted reduction, retains 10. Fertilized eggs have 10+10
and give rise to females; the same eggs unfertilized develop
parthenogenetically into males with a set of 10 maternal
chromosomes.
These cytological findings are in harmony with the sex-
linked mode of inheritance displayed by certain mutant
forms. Thus when a female with the recessive mutant orange
30
HABROBRACON 3I
eye-colour is mated with a wild-type male (black eye-
colour) the daughters are black-eyed and the sons orange-
eyed.
But it was found that in matings in which the orange-eyed
mother and the black-eyed father were from the same stock
or from stocks closely related through inbreeding, black-
eyed sons appeared. By genetical experiment and by cyto-
logical examination these were shown to have received a
chromosome set from both the father and the mother, having
20 altogether and being heterozygotes.
The hypothesis elaborated to account for these 'biparental
males' rests on the assumption that the normal female is a
heterozygote in respect of two sets of multiple sex alleles or
differential chromosome segments which for purposes of
discussion may be designated X^ and X^ respectively. There
are two kinds of the normal haploid male, X^ and X^. The
'biparental male' is aX^iaA or aX^iaA, with the same
genie balance as the ordinary haploid male X^:A or X^:A.
The normal diploid heterozygous female is X^:A/X^:A.
So that the male is N^ or N^, the female NVN^, and the
'biparental male' N^/N^ or N^/N^.
The fact that inbreeding yielded a marked increase in the
production of 'biparental males' resisted satisfactory ex-
planation for a long time (Bostian, 1934; Whiting, 1935;
Snell, 1935). Ultimately Dordick( 1 937) was able to show by
a number of ingenious experiments that the low incidence
of biparental males (i such to 9 biparental females in the
ordinary laboratory stocks) was due to the conversion by
gene action of the biparental male into a female, the gene or
genes concerned being resident not in the X but in another
chromosome, the so-called Z. Thus in Habrobracon the
existence of multiple sex-differentials in different chromo-
somes was disclosed and the notion of genie balance shown
to apply.
Dreyfus and Breuer (1944) found in another parasitic
wasp Telenomus fariai a special chromosome mechanism
which makes inbreeding compatible with a method of sex-
determination resembling that in Habrobracon.
In the Iceryini the sex-determining mechanism is of the
32 SEX-DETERMINATION
haplo-diploid type. The genie balance concept of sex-
determination cannot be applied since the ratio of male-
determining to female-determining genes is the same both
in the haploid male and the diploid female. Formal explana-
tion is possible by means of the hypotheses advanced by
Goldschmidt (1920) and by Schrader and Sturtevant (1923).
The former suggests that precocious activity by the male-
determining genes in the diploid dose and prior to reduction
predispose all eggs to a male pattern of sexual differentia-
tion and that this is then overridden in fertilized eggs by
the delayed activity of two sets of female-determining
genes. But this 'turning-point' hypotheses is not gener-
ally accepted. The algebraic sum hypothesis of Schrader
and Sturtevant, helpful and ingenious as it is, is not suitable
for general application.
Sciara. Metz (1938) and his colleagues studied the genetic
and cytological aspects of sex-determination in the dipteran
fungus-gnat Sciara coprophila over a long period of years
and have recorded much that is remarkable. A given female
produces offspring predominantly of one sex. Among the
families in which most of the progeny are females there are
two types of females, female-producers and male-producers,
indistinguishable on inspection and in respect of the be-
haviour of their chromosomes. They differ genetically,
however. The female-producers may be designated XX^,
being heterozygous for a gene in the X, and the male-
producers as XX, being homozygous for the recessive allele
of this gene. Males are genetically XOiAA in somatic con-
stitution and produce one type of sperm, XXA. A given
female produces the same kind of offspring, whether sons
or daughters, irrespective of the origin of the male to which
she is mated.
The mode of inheritance of certain mutant characters is
peculiar. Metz (1927) used an autosomal recessive mutant
truncate wing. Truncate $ x wild-type ^ gave none but
wild-type. Some of the F^ families were mostly daughters,
others mostly sons. F.i o x homozygous truncate ? gave
all truncate, daughters in some families, sons in others. But
LYMANTRIA DISPAR 33
when truncate male was mated to a wild-type female and
the F.I wild-type males back-crossed to truncate females,
all the offspring were wild-type. The male had transmitted
to his offspring only that allele which he had received from
his mother. This matroclinous inheritance manifestly differs
from sex-linked inheritance for the character truncate is
distributed alike to both males and females.
Metz and Schmuck (1929), using a sex-linked recessive
mutant swollen wing, found that swollen (^ x wild-type ?
gave all wild-type in F.i and that in F.2 swollen reappeared
in half the sons in the male families but in none of the
daughters of the female families. Sw^oUen ? x wild-type ^
gave swollen sons, the swollen females all proving to
be male-producers. Thus the mutation had occurred in
the X and had not passed into the X^ through crossing-
over.
A dominant mutant gene 'Wavy' was found by Metz and
Smith (193 1 ) to have occurred in the X^ and not to have
crossed over into the X.
Thus it would seem that female-family-production is a
character determined by a dominant gene in the X chromo-
some (X^) and that male-family-production is a character
based on the recessive allele of this gene.
The reason for this matroclinous inheritance — the male
transmitting to his progeny only those genes, sex-linked and
autosomal, that he himself received from his mother, his
spermatozoa lacking the paternal chromosomes — has been
revealed by cytological investigation (Du Bois, 1932).
Femaleness in Sciara is determined by the genie balance,
2X:2A=femaleness; iX:2A=maleness. The dominant gene
(X^) acts by so conditioning the cytoplasm that in the
X^X:2A constitution one paternal X is eliminated from the
nucleus. The XX:AA constitution leads to the elimination
of two paternal X's and to the soma of the male becoming
XO:AA.
Lymantria dispar. The term intersex was first used by
Goldschmidt in 1925 to describe certain sexually aberrant
types that he had described in 191 1 and which had appeared
34 SEX-DETERMINATION
among the offspring of the mating of European Lymantria
females and Japanese Lymantria males. This mating gave
normal sons and individuals showing a mixture of male,
female and intermediate characters.
It has long been known to entomologists that crosses
between different geographical varieties of the Gypsy moth
sometimes yield these sexually aberrant forms. This inter-
sexuality is in no way associated with any corresponding
abnormality in respect of chromosome number or be-
haviour. The female is the heterogametic sex. Goldschmidt
(1920, 1 93 1, 1934) was able to classify the intersexes
according to their characterizations into two main types,
male intersex and female intersex, the former being an XX
individual which exhibits female as well as male characters,
the latter an XY individual with both female and male
characters. The intersex is a sex mosaic. The female inter-
sexes range from the unexceptional female, through
increasing grades of intersexuality — i.e. with increasing
degrees of maleness — to complete sex-reversal — i.e. an XY
individual that is a functional male. A corresponding series
of male intersexes ranges from complete maleness to
complete femaleness.
A careful examination of great numbers of intersexual
individuals permitted Goldschmidt to conclude that there
was indeed a time seriation of events in the development of
the sex-characters — that is to say, that all the structures of
the sex equipment were not differentiated at any one time
but that one structure of this equipment appeared before
another, and so on, and that the grade of intersexuality was
determined by the relative number of these structures that
were male and female in type respectively. It appeared that
the last structure of the sex-equipment to become differ-
entiated in the life history of the individual was the structure
most commonly affected in this process of intersexuality,
and that a greater number of these structures became
affected with each increasing grade of intersexuality.
The original matings on the results of which Gold-
schmidt's hypothesis is founded were as follows:
LYMANTRIA DISPAR 35
European? x Japanese o=F.i: all sons normal, all daughters
intersexual
F.2: all sons normal, half daughters
normal, half intersexual (the
grade of intersexuality being as
that in the mother. Only the
lower-grade intersexuals could
be bred from)
Japanese ? x European o =F.i: sons and daughters all normal
F.2: all daughters normal, half sons
normal, half intersexual
For purposes of description and discussion Goldschmidt
refers to the Japanese race in these experiments as a 'strong'
race, and the European as 'weak'. Female intersexuality is
produced in an F.i when a 'weak' female is crossed with
a 'strong' male. Male intersexuality is exhibited by a pro-
portion of males in the F.2 of the cross 'strong' female x
*weak' male. From these results it is seen that sex-determina-
tion is a phenomenon partaking of the nature of a genie
balance, sex being dependent upon a particular relation of
certain determiners, their relative 'strength' or 'weakness';
in other words, a balance or lack of balance of these deter-
miners. It is clear that these determiners are of two kinds,
one of which shifts sex toward the female type, the other
toward the male.
In order to determine how these sex-determining factors
were transmitted, Goldschmidt carried out the following
breeding experiments:
A. F.I weak 2 x strong o gave cj'cJ all normal and ?? intersexual
F.2 weak $ x strong o gavecJcJ all normal; ?? half normal, half
intersexual
Backcross. Weak $ x F.i (weak ? x strong <^) o gave ob*
normal; 2$ half normal, half intersexual
Backcross. Weak $ x F.i (strong $ x weak (J) o gave 36
normal; ?? half normal, half intersexual
Backcross. F.i (weak ? x strong o) ? x weak ^ gave cJcJ all
normal; $2 all normal
Backcross. F.i (weak ? x strong o) ? x strong o gave S6 all
normal; ?$ all intersexual
In all these crosses it is the maternal line that is 'w^eak'. The
results show at once that the 'strength' which produces
36 SEX-DETERMINATION
female intersexuality is transmitted in the X-chromosomes,
and the resuhs are exactly what would be expected if this
intersexuality-producing 'strength' is a property of the
X-chromosome of the 'strong' race. They show, further,
that the X-chromosome of the 'weak' race carries the
determiner of this property 'weakness', and, finally, they
show that the F. i females behave like pure 'weak' females.
B. F.I strong $ x weak cJ gave $$ all normal; ^(^ all normal
F.2 strong $ x weak (^ gave $$ all normal; (^<^ half normal,
half intersexual
Backcross. Strong $ x F.i (strong $ x weak cJ) (^ gave ?? all
normal; ^<^ all normal
Backcross. Strong $ x F.i (weak ? x strong o) o gave 2$ all
normal; SS all normal
Backcross. F.i (strong $ x weak (J) $ x strong (J gave $$ all
normal; c^cJ all normal
Backcross. F.i (strong $ x weak cj") $ x weak (^ gave ?? all
normal; dl*c? all intersexual
These results show that the property 'weakness' (weak
males) is transmitted in their X-chromosomes, that in these
combinations two 'strong' X-chromosomes or one 'strong'
and one 'weak' produce normal males, two 'weak' X-chromo-
somes produce intersexual males, and that all the mothers
in this series behave as 'strong' females whether they belong
to a pure strong race or whether they be hybrids out of a
'strong' mother and a 'weak' father.
If the two lots of results are considered together it is seen
that 'strength' and 'weakness' are, firstly, characters, the
determiners of which are carried in the X-chromosomes of
the respective races, and, secondly, that 'strength' and
'weakness' are properties which are inherited only in the
female line. Sex is determined by a definite relation or
balance between the respective 'strength' or 'weakness' of
one type of sex-determining factors inherited maternally
and the other type which are transmitted within the
X-chromosomes. It is seen, further, that the combination
of the 'weak' maternally inherited determiner with a
'strong' X-borne determiner shifts the female (XY) toward
maleness, whereas the combination of a 'strong' maternally
LYMANTRIA DISPAR 37
inherited determiner with two 'weak' X-borne determiners
shifts the male (XX) toward femaleness. It follows, there-
fore, that the X-chromosomes must contain male-determin-
ing factors, 'strong' in the 'strong' and 'weak' in the 'weak'
races, and that the female-determiner also 'strong' in the
'strong' and 'weak' in the 'weak' races, is not to be found
in the X-chromosome but elsewhere. Goldschmidt has
adduced reasons for the view that the female-determining
factor is resident in the Y-chromosome. Thus sex in the
Gypsy moth, he suggests, is determined by a relational
balance between a maternally inherited (Y-borne) female-
determiner (F) and a male-determiner (M), of which one is
present in the female and two in the male, and which
is borne in the X-chromosome. Intersexes appear if in
a hybrid combination of M and F these sex-determining
factors are not properly balanced. Goldschmidt regards the
M and the F as being single genes for the reason that never
in thousands of crosses has any result been obtained which
would support any other conclusion.
His results can be illustrated in simple fashion by the
following scheme: In the Gypsy moth the male has a sex-
chromosome constitution XX, while the female is XY. The
male-determining genes are resident in the X-chromosomes,
the female are in the Y and are therefore restricted to the
maternal line. But Goldschmidt gained evidence which
forced him to the conclusion that the female-determining
factors borne on the Y-chromosome acted prezygotically —
that is to say, before the X and the Y chromosomes in the
naturing egg had separated. The physiological effects of the
action of these Y-borne genes would thus pervade the whole
of the immature egg. Two kinds of eggs would be produced,
an X-bearing egg, the Y-chromosome having passed into
the polar body, or a Y-bearing egg, the X-chromosome
having passed into the polar body, but, in respect of the
female-determining reactions which result from the func-
tioning of the Y-borne gene, the X-bearing egg and the
Y-bearing egg produced by the same female are exactly
alike.
A male like a female has its origin in an egg, but in the
38 SEX-DETERMINATION
union of an X-bearing sperm with an X-bearing egg. Since
this egg is already endowed with female-determining pro-
perties of a certain valency, the symbol for male must be
(MX)(MX)F whilst that for a female is (MX)F. In order to
simplify the symbols it is convenient to leave out the X and
to indicate a male by the formula MMF and a female by
MmF (the small m indicating that only one X chromosome
is present). The female-producing tendency of the cyto-
plasm F can be overcome by MM but not by M, and so in
each generation equal numbers of normal males and females
are produced in the case of each pure race of Lymantria.
The explanation of the appearance of intersexes on crossing
different races turns upon the assumption that the intensity
of the action of M and F differs in different races. The M
and F in L. japonica are stronger, and exert their influence
earlier in the course of development, than the M and F of
L. dispar.
The relative 'strength' and 'weakness' of the sex-deter-
mining genes can be indicated by assigning to the M and F
numerical values, e.g. M5 is much stronger than M3, and
M3 than Mj. F^ is much weaker than F3, and Fg weaker
than F5. Now, consider the mating of a 'weak' female
(MamFg) to a 'strong' male (M5M4F4). (It will be noted
that the male-determining factors of the male have a different
valency. This is possible since the two X-chromosomes
which carry these come from different parents which may
differ in respect of the valency of their sex-determining
factors.) The female will elaborate two kinds of eggs — one
M2F3 and the other mFg. The male will elaborate two kinds
of sperm — M5 and M4. It is to be noted that the female-
determining factors are restricted entirely to the female line.
These four kinds of gametes, two from each side, will pro-
vide the following types in the F^: M5M2F3; M5mF3;
M4M2F3; M^mFg.
Now, sex is determined by that kind of sex-determining
reaction which is in effective excess. In the case of the
M5M2F3, M=7, F=3— that is, M is greater than F. The
sex-chromosome constitution is XX and therefore this
individual is a normal male. In the case of the class M5mF3,
LYMANTRIA DISPAR 39
M is greater than F, so that in spite of the fact that this
individual is XY in sex-chromosome constitution, that is,
genetically a female, it will be intersexual; in fact, according
to the argument it will be a genetical female completely
transformed into, and functioning as, a male. Individuals
M4M2F3 are normal males, whilst those which are M^mFj
are genetically females, but nevertheless are females trans-
formed into males.
A survey of the Central European and Japanese races of
Lymantria has provided Goldschmidt with different strains
which possess all kinds of combinations of 'strong' and
*weak' male-determining factors, with 'weak' and 'strong'
female- determining factors, and by the use of them he was
able to produce any percentage of intersexual forms and
any grade of intersexuality, either male or female, at will.
Whilst in Japan Goldschmidt was enabled to distinguish
eight different strains of Lymantria, and an elaborate series
of breeding experiments permitted him to arrange them in
a series of decreasing strength. The differences between the
extremes of this series were greater than those between the
European dispar and the L. japonica which he first used.
Indeed, it was so great that when a 'strongest' father was
mated with a 'weakest' mother, the progeny consisted solely
of males, half of these being chromosomally males MgMgF,
whilst the rest were really females MgmF in which the
male- determining factor, introduced from the strong race,
had overwhelmed the female-determining factor of the
weaker. The 'strength' or 'valency' of the sex factors differed
for each race; but in each race it was fixed. Goldschmidt
holds the view that this fixity is really quantitative, depend-
ing upon definite amounts of the sex-determining material
present in any case. He has satisfied himself that the differ-
ent degrees of strength and weakness of these sex-deter-
mining factors reveal the existence of a series of multiple
allelomorphs, but, more recently, he has been forced to the
conclusion that in the case of the mating 'strong' Japanese x
'weak' European a pair of autosomal allelomorphic modify-
ing genes is involved which affects the expression of male
intersexuality. Goldschmidt's results show that the different
40 SEX-DETERMINATION
conditions of the male- and the female-determining factors
of the different races form an orderly quantitative series in
regard to their effect and that different possible combina-
tions behave exactly as if the different degrees of strength of
these genes could be expressed in numerical values.
The genetical basis of sex and intersexuality as under-
stood by Goldschmidt is given by the amount of balance
or imbalance between M and F at the beginning of develop-
ment. In the uneventful differentiation of the normal male
M is always effectively in excess of F; in the case of the
normal female F is at all times effectively in excess of M,
but in the development of the intersex the relationship of
M and F is disturbed; M (or F) overtakes and replaces
F (or M) at some point — the turning-point or switchover.
The effect of this genie situation is that at a certain moment
in development the switch-over occurs and the control of
the remaining events in sexual differentiation is shifted from
the F to the M genes, or vice versa, and the time of occur-
rence of this event is the simple function of the relative
degree of balance or imbalance between F and M. It would
seem that M and F respectively are responsible for sex-
determining reactions which proceed with a velocity pro-
portional to the strength or valency or quantity of these
genes; that the quicker reaction controls the sexual differ-
entiation and that the two curves of M and F reactions may
have points of intersection, that is, at the switch-over, if the
quantities of M and F are not properly matched. If this is
so, then it should be possible to produce abnormal forms by
changing the relative velocities of these two reactions within
a pure normal race, through the differential action of
temperature, for example. This Goldschmidt has done with
positive results, producing intersexuality by the action of
extreme temperature within a pure race.
Winge (1937) offered an alternative explanation of the
observations that required Goldschmidt to postulate cyto-
plasmic inheritance. He suggested that the X-chromosome
contains a preponderance of male-determining genes,
strong (M 50) in the Japanese variety and weak (M 10) in
the European; that the Y has a preponderance of female-
LYMANTRIA DISPAR 4I
determining genes, very strong (F 70) in the Japanese
variety and weak (F 24) in the European; that all the
autosomes carry sex-determining genes, some male- and
some female-determining, and that in the Japanese variety
the autosomal female-determining genes are strong (F 20)
and weak in the European (F 4).
By the use of these assumptions, which are exactly like
those made by Goldschmidt himself elsewhere, all reference
to the c\1;oplasm can be avoided and the facts of sex-
determination in Lymantria can be brought into line with
the rest.
Baltzer (1937), who for many years had been studying
problems of sex-determination and of intersexuality in
Bonellia viridis, found himself unable to accept Gold-
schmidt's notion of the turning point or switch-over.
This marine worm in its larval form floats on the surface
of the sea. When it settles on or near the proboscis of an
adult female it thereafter pursues a male differentiation.
If, on the other hand, chance leaves it far removed from an
adult female, it becomes a female. If the young individual,
having begun to differentiate as a male, is removed to a
distance from the adult female its differentiation switches
to the female pattern and an intersexual form results. It has
been shown that there is a chemical substance in the female's
proboscis which dominates the sexual differentiation of the
young individual.
These events relate to the physiology of sex-differentia-
tion and not to the phenomenon of sex-determination.
There may or may not be a chromosomal, genetic, sex-
determining mechanism in Bonellia. If there is it is over-
ridden by an external chemical influence.
Baltzer is satisfied that in the intersex of Bonellia there is
no purely male development period followed by a female de-
velopment period but that the intersexual organs are inter-
sexual from the beginning.
CHAPTER 5
GENITIC INTERSEXUALITY IN DROSOPHILA,
CERTAIN LEPIDOPTERA AND BIRDS
Drosophila. The first description of a gene in Drosophila
which profoundly affected the sexual characterization was
that given by Sturtevant (1920) in D. simulans. In a par-
ticular stock it was noted that many individuals exhibiting
a definite intersexual condition appeared. They were
sterile, but the mating of their apparently normal brothers
and sisters to unrelated stocks commonly produced the
same abnormal forms in the Fg generation, the sex-ratio
being of the order of 4 males; 3 females, i intersex, which
suggested that these intersexes were modified females. By
the use of sex-linked genes Sturtevant was able to demon-
strate that this was so, and further breeding experiments
showed that the agent responsible was a recessive gene
resident in the second chromosome.
In Drosophila virilis Lebedeff (1934) found a third
chromosome recessive gene which transformed the XX
individual into a sterile male but left the XY individual
unaffected. Later (1937) Lebedeff showed that the XX
individual began its development according to the female
pattern and that later male organs made their appearance,
the two sets, male and female, continuing thereafter to
develop side by side.
Bridges (1921, 1922, 1925) described a form of inter-
sexuality in Drosophila melanogaster caused by an altered
ratio of sex-chromosomes and autosomes. These intersexes
showed complex mixtures of male and female parts. They
could be produced by breeding from certain of their sisters
which were to be distinguished by their large coarse eyes,
thick-set bodies, coarse bristles and hair pattern on the
wing. Cytological examination demonstrated that these
intersex-producers were triploids, every chromosome being
present in triplicate (3N). All the eggs produced by them
42
GENETIC INTERSEXUALITY IN DROSOPHILA 43
contained one full set of chromosomes and part or all of an
extra set. The diploid (2N) eggs fertilized by X-sperm gave
rise to 3N females; fertilized by Y-sperm they gave the
intersexes which were 2X:3A as contrasted with the 2X:2A
normal female (X=X chromosome; A=one haploid set of
autosomes).
These observations made it clear that sex was determined
not, as had been thought, by the presence of one X or two,
but by the balance between the X and the autosome material,
by the genie balance. Dobzhansky and Bridges (1928) car-
ried this w^ork to its conclusion to find that X>A, i.e. that
the net male-determining tendency of a set of autosomes is
less than the next female-determining tendency of an X.
iX:2A=a male
2X:2A=a female
If the female-determining tendency of the sex-determin-
ing genes in an X-chromosome is represented by the figure
100, then the net male-determining tendency of the sex-
determining genes in a set of autosomes is of the order of 80.
iX:2A
100 160
2X:2A
200 160
The following abnormal types could be expected and
were to be explained as under:
Sex-type
Formula
X=ioo
A=8o
Sex-index
Superfemale
2N
3X:2A
300
160
1-88
Female
4N
4X:4A
400
320
1-25
3N
3X:3A
300
240
1-25
2N
2X:2A
200
160
I 25
iN
iX:iA
100
80
I 25
Intersex
4N
3X:4A
300
320
0-94
3N
2X:3A
200
240
0-83
Male
2N
iX:2A
100
160
0-63
4N
2X:4A
200
320
0-63
Supermale
3N
iX:3A
100
240
0-42
44 SEX-DETERMINATION
Most of these sex-types have been encountered and have
been found to conform with the predictions made.
Sex-determination would therefore seem to be the end
resuh of a quantitative balance between X-chromosomes
and autosomes. In Drosophila melanogaster the X is not a
determiner of sex but is a differential. The genes that are
concerned in sex-determination are scattered irregularly
throughout all the chromosomes, sex-chromosomes and
autosomes alike. In a general way these genes are to be
classified as female- and male-determining and the two
types are in a way opposed to each other. In the X the genes
for femaleness preponderate over those for maleness so that
this chromosome is, on the whole, female-determining. In
the second and third chromosomes the male-determining
genes preponderate over the female-determining genes and
these chromosomes therefore are on the whole male-
determining. The fourth chromosome is mainly female-
determining.
*Both sexes are due to the simultaneous action of two
opposed sets of genes, one set tending to produce the
characters called female and the other to produce the
characters called male. These two sets of genes are not
equally effective, for in the complement as a whole the
female-tendency genes outweigh the male-tendency genes,
and the diploid (or triploid) form is a female. When the
relative number of the female-tendency genes is lowered by
the absence of one X, the male-tendency genes outweigh the
female, and the result is the normal haplo-X male. When
the two sets of genes are acting in a ratio between these two
extremes, as in the ratio of 2X13 sets of autosomes, the result
is a sex-intermediate — the intersex.'
The use of fragments of the X- duplications of various
lengths and from different regions of the chromosome and
of deficiencies of the X by Dobzhansky and Schultz (1934)
provided experimental proof of these assumptions.
Lepidoptera. Standfuss (1908) crossed Saturnia pyrt and
S. pavonia and then back-crossed the F. i males to S. pyri
females to get 42 males and 38 'gynandromorphs'. Federley
GENETIC INTERSEXUALITY IN BIRDS 45
(19 1 3) mated Pygaera anachoraeta females with P. curtula
males and back-crossed the F.i males to P. anachoraeta
females to get similar 'gynandromorphs'. He then examined
his material cytologically to find that the haploid number
for P. anachoraeta is 30 and for P. curtula 29. In the
spermatogenesis of the F.i males all 59 chromosomes
divided equationally so that the 'gynandromorphs' received
59 chromosomes from their hybrid father and 30 from their
mother. They were triploids 2X:3A (possibly +Y).
Seiler (1937) obtained similar triploid intersexes in the
F.I of the mating of females of the tetraploid (4N=i2o)
parthenogenetic variety of Solenohia triquetrella with males
of the diploid (2n=6o) bisexual Niirnberg variety of the
same species. The intersexes had 90 chromosomes and
showed a mixture of male and female parts of varying
degrees of development. Seiler found no support in his
material for Goldschmidt's 'turning point' hypothesis.
Birds. That sex-determination in the fowl is likewise a
matter of a quantitative balance between sex- and auto-
somes was strongly suggested by Crew and Munro's (1938,
1939) studies of gynandromorphism and lateral asymmetry
in birds. Several instances of lateral gynandromorphism in
the fowl have been reported. In such the size difference
between the two sides of the body can be of the order of
10-15 per cent, and the gonads are different, one being a
testis the other an ovary or ovo-testis. The explanation
offered was that non-disjunction of an autosome had
occurred to result in bilateral heteroploidy, there being the
gain of an autosome on the larger side, its loss on the smaller,
and that this disturbance of the quantitative balance be-
tween sex- and auto-somes was responsible for the gonadic
differences.
CHAPTER 6
SEX-DETERMINATION IN FISH AND
THE LOWER ALGAE
SEX IN PARAMECIUM AND FUNGI
SEX-DETERMINATION IN BRYOPHYTES
SEX IN THE HIGHER PLANTS
Fish. The identification of the sex-chromosomes in fishes is
difficult, but the evidence derived from genetic experi-
mentation with Lebistes, Aplocheilus and Platypoecilus
has shown that in some species the male is the hetero-
gametic sex and that in others he is homogametic.
Winge (1922, 1934) has produced convincing evidence
that in Lebistes reticulatus there are several mutant genes in
the Y-chromosome. Spot, a large black spot on the dorsal
fin, is a character exhibited by a certain geographical
variety of this fish. Spot (^ x 5 of a variety lacking this
spot=F.i and F.2 spot males. Non-spot (^ x 5 of a spot
variety=F.i and F.2 non-spot males. The character of the
father is transmitted to all his male descendants. Winge
explained this by postulating that the male was XY and
that the spot gene was Y borne.
Since then Winge has described eight other characters
that in inheritance behaved like spot. He has also described
eight other recessive characters, patterns of male coloration,
the genes for which are presumably resident in the X for the
characters were not exhibited by the F. i but reappeared in
50 per cent, of the males in F.2. Occasionally, however, an
F.I male exhibited the character. Winge explained this by
postulating that the X was homologous to a portion of the Y
and that crossing-over had occurred between these homo-
logous parts. When such an exceptional F.i male was used
in breeding, all his sons displayed the character.
In two varieties Winge observed a marked inherited
tendency toward the production of females with male-like
gonopodia and remarkable in that in them the heterozygous
46
FISH 47
characters with genes in the X showed up faintly. He inter-
bred these varieties and obtained a small proportion of XX
individuals (according to the genetical evidence) that were
males in appearance, behaviour and function.
When these XX males were mated all of their progeny
turned out to be females. The father mated to his daughters
gave none but females. Mated to some of these new
daughters he produced a completely male individual among
the progeny. When this new male was mated with his sisters
about half of the offspring were males.
In this way Winge produced a new kind of male, XX
instead of XY. The X was no longer the sex-diiferential and
the characters based on X-borne genes were exhibited by
both sexes, behaving as characters based on autosomal-
borne genes. The new fish was XX male; XY female; but
the sex- differential function had been assumed by an auto-
some through the accumulation in it of male-determining
genes.
It now became possible for Winge to produce YY sons
who inherited the Y-borne characters from both father and
mother.
Winge concludes that male-determining and female-
determining genes are scattered throughout the autosomes
and sex-chromosomes alike and that sex-determination is
the outcome of the specific balance betw^een the two
kinds.
Aida (192 1, 1930, 1936), working with the Japanese
Killifish Aplocheilus latipes, obtained results completely
parallel with those of Winge and offered a similar inter-
pretation.
The genetical evidence relating to the Mexican Killifish
Platypoecilus maculatus and obtained by Bellamy (1928)
pointed directly to the conclusion that in this species, in
contrast to Lebistes, the female is the heterogametic sex
and that crossing-over occurred between the X and the Y.
In two broods Chavin and Gordon (1951) obtained none
but males. The female parents were XX, the male YY, so
that all the offspring were XY, which is characteristic of the
normal male in this strain.
48 SEX-DETERMINATION
Lower Algae. Hartmann and his colleagues (1932) have
shown that different strains of the unicellular Chlamydo-
monas eugametos can be classified into two groups, desig-
nated plus and minus. Plus cells never unite with plus and
minus never unite with minus. In certain conditions a plus
cell fuses with a minus cell to form a diploid zygote. This
undergoes two meiotic divisions and gives rise to 4 haploid
zoospores, two of which belong to the plus and two to the
minus types. They behave therefore as though they were
different and contrasted sexual forms.
Paramecium. Sonneborn (1947) and others have shown
that several species of Paramecium and one species of
Euplotes are divisible into mating types between which,
but not within which, conjugation takes place. Within a
species there can be anything up to eight of these mating
types. If, therefore, these mating types are regarded as
sexual types they provide examples of the phenomenon of
multiple sexuality which is encountered also among the
algae and fungi.
Fungi. Blakeslee (1904) showed that in the bread mould
Mucor zygospores are sometimes formed by the union of
hyphae from the same mycelium, being homothallic, but
that in most instances zygospores are formed only when two
distinct mycelia come together, these mycelia being sexually
different or heterothallic. Within a given heterothallic
species every individual can be assigned to one of two types
plus and minus. Two plus individuals will not unite
sexually, neither will two minus individuals. It is when
plus and minus mycelia come in contact that zygospores are
produced.
Bryophytes. In most of the bryophytes the gametophytes
are haploids, being of two kinds, one female (XA) and the
other male (YA). In 1917 Allen described the large X and
the small Y of Sphaerocarpus donnellii in which the haploid
female gametophyte has seven autosomes and a very large
X, the male gametophyte seven autosomes and a very
THE HIGHER PLANTS 49
small Y. Since then (Allen, 1936) some thirty other bryo-
phytes have been shown to have distinguishable sex-
chromosomes.
Mackay and Allen (1936) have found X:2A and 2X:2A
female gametophytes and 2Y:2A male gametophytes in
Sphaerocarpus. But gametophytes with the constitution
XY:2A were found to be intersexes. Similar polyploids
described by Knapp (1936) indicated that the male-deter-
mining genes preponderate in the autosomes and that the
Y was neutral.
The Higher Plants. Sex-chromosomes have been dis-
covered also in the angiosperms. Santos (1923) found 24
matched pairs of chromosomes in the female and 23 matched
pairs and an unequal XY pair in the male of the dioecious
Elodea gigantea. Since then some fifty dioecious angiosperms
have been shown to have distinguishable sex-chromosomes
and in some twenty other dioecious species no such discern-
ible difference could be detected. It would appear that, as
a rule, in these dioecious species the male is the hetero-
gametic sex. Only in one of them was the female the hetero-
gametic sex and only in one, Dioscorea siniiata, was the male
found to be XO,
Sex-linkage has been encountered in Melandrium (Baur,
1912; Shull, 1914). In this form Winge (1923) found a visibly
distinct XY pair of sex-chromosomes in the male, the female
being XX. Other sex-linked characters in Melandrium have
been described by Winge (193 1), who showed that crossing-
over between the X and the Y occurred.
The monoecious (haemophroditic) Bryonia alba is closely
related to the dioecious (bisexual) B. dioica. Correns (1907)
found that the cross B. dioica 2 by the pollen of B. alba
gave only females, occasionally with a few^ male flowers.
The reciprocal cross B. dioica (^ x B. alba pistillate flowers
gave females (with an occasional male flower) and males in
equal numbers.
There are no visibly distinguishable sex-chromosomes in
either of these species (Meurman, 1925). The hybrid pro-
geny are all sterile.
50 SEX-DETERMINATION
These results can be explained on the following assump-
tions: {a) 2X:2A=$XY:2A=(^, (b) in B. alba, which is a
homozygous strain, all individuals are females modified to
give staminate flowers by a male-determining mutation in an
autosome, {c) XX:A°iA°i=hermaphrodite. All the progeny
of the cross B. dioica ^ x B. alba (^ would be XX:AA°i and
are females with a tendency to produce male flowers. In the
reciprocal cross the females would be XXiAA^^ but the
males would be XY:AA°i and therefore 'stronger' than
B. dioica males.
In maize, which is normally monoecious, a dozen and
more mutations have been found which modify the expres-
sion of sex (Emerson, 1924, 1932). By the use of certain of
these dioecious strains of maize have been produced. These
mutants provide strong support for the conception that the
sex-characters are the product of the action of many genes,
some male-determining and some female-determining, the
end result being decided by the interplay between these two
kinds.
In Rumex acetosa Ono (1935) has described the occur-
rence of triploidy. The normal diploid female has 14
chromosomes, XX:6 pairs of autosomes. In the male there
are the same 6 pairs plus XYY. Individuals with the con-
stitution 2X+2Y+3A were found to be intersexes. In this
species the sex-determining genes on the X are pre-
dominantly female-determining, those on the autosomes
predominantly male-determining, and the Y is neutral.
CHAPTER 7
SPECULATIONS CONCERNING THE EVOLUTION
OF THE SEX-DETERMINING MECHANISM
It is possible that at a certain stage in the history of the
earth the conditions essential for the appearance of life pre-
sented themselves, never afterwards to be repeated, peculiar
in respect of temperature, pressure, of the composition of
the waters and of the gases in the atmosphere above the
waters. It is possible that the conditions at that time exist-
ing led to the appearance of living matter as inevitably as
earlier and different sets of conditions had led to the form-
ation of the seas and the rocks.
The first living or half-living things which appeared in
the waters were possibly large molecules synthetized under
the influence of the sun's radiation and capable of repro-
duction only in this particularly favourable medium.
A review of living things now^ known to us permits us to
assume that the enzyme, the virus and the bacteriophage
are perhaps milestones along the beginning of the road that
life has passed onwards and upwards toward its inevitable
destiny. If they cannot be seen they can be recognized
and counted by the effects they produce. Muller (1929) has
suggested that the bacteriophage is a gene.^ It may well be
that life remained in this stage of its development for many
millions of years before a suitable assemblage of similar
units was brought together in the first cell. There must have
been innumerable failures, but the first successful cell which
consisted of numerous half-living chemical molecules
suspended in water and enclosed in an oily film found plenty
of food and an immense advantage over its competitors.
From this original simple colloidal complex to the first and
simplest unicellular organism known to the biologist is a
^ For a fuller account of bacteriophage and of its nature the
reader is referred to Dr. Gardner's excellent monograph on
Microbes and Ultramicrobes in this series.
51
52 SEX-DETERMINATION
Step as vast as that which separates the latter and man. We
know nothing of this grand procession; we can but con-
jecture that it was punctuated by the development of various
precise mechanisms. From what we know of the gene today
we can surmise that the earliest genes consisted of molecules
capable of determining the formation of similar particles
and also of dissimilar particles. We may assume that repro-
duction by simple division attended upon growth and that
every few hours a new generation of these units was sub-
jected to the appraisal of the selecting factors in the changing
environment. At some stage in this eventful history there
must have come a time when the gene, dividing, became
two which did not separate but which remained together so
that the beginnings of a gene company would be evolved.
Since we know that genes in such a company can mutate
independently, it follows that through the increasing com-
plexity thus resulting advantages possessing a survival value
would be conferred upon the individual.
The benefits of gene association must then have been
made more permanent by the development of mitosis,
which development would take the form of the establish-
ment of a mechanism which ensured the synchronous
division of all the genes. Thus the nucleus would be evolved
and within it the gene associations would become linear and
the chromosomes would be formed, and, for their exact
division, the centrosome, spindle and the spindle attach-
ment would be evolved. Fragmentation, with the develop-
ment of new spindle attachments, translocation, together
with frequent gene mutation, would slowly, surely, build
up permanent gene associations which would yield different
types of genie balances to be appraised and selected. At this
stage, sexual reproduction would appear, possibly as a
result of a gene mutation which made the fusion of two
individuals inevitable. Following upon this, meiosis — a
modification of mitosis — must have appeared, bringing with
it two exceedingly great advantages; the maintenance of
constancy in chromosome number and the provision of the
conditions of crossing over with consequent recombination
of genes and reconstruction within the chromosome. It may
EVOLUTION OF MECHANISM 53
be assumed that originally this modification of mitosis
applied to all mitoses in the organism. Later developments
would be restriction of meiosis in time and in space.
Ultimately, as living types evolved, it would be restricted
to certain events in gametogenesis, and the gametes would
come to be constitutionally haploid cells, and the diploid-
haploid mechanism would be perfected.
Next, it may be assumed, came a differentiation of the
gametes to yield one kind that was fertilized and another
that fertilized. Then followed the development of homo-
hetero-gamety, one type of individual becoming so equipped
that perforce it must elaborate two kinds of gametes. This
probably was affected by development which reduced
crossing over. It is established that, in Drosophila at least,
there are genes which can and do reduce or even suppress
crossing-over. The suppression of crossing-over means that
qualitative differences can arise in the members of a chromo-
some pair, and that these cannot be transferred from one
member of the chromosome pair to the other, so that in
respect of these qualitative differences the individual
maintains a constitutionally heterozygous condition. It is
established, further, that reduction of crossing-over in the
case of one pair of chromosomes is attended by a similar
reduction of crossing-over in the case of all the rest of the
chromosomes within the chromosome complex. It may be
assumed that this suppression of crossing-over occurred in
the case of a pair of chromosomes which later were to
become the sex-chromosomes. As a result of this suppres-
sion, two chromosomes would evolve independently of one
another and would ultimately come to lose all qualitative
relationship. Following upon this would come quantitative
differences between the members of the sex-chromosome
pair. At first the members of this pair would be alike in
external structure. Part of one of them which, because of a
non-homology, could no longer pair with the corresponding
portion of the other, would become deleted so that there
would now remain an X-chromosome and a Y. The
Y-chromosome, by further deletion, would become smaller
and smaller, and finally the whole of it would be eliminated.
54 SEX-DETERMINATION
The qualitative-quantitative differentiation of the sex-
chromosomes has actually been observed in every stage of
development from their behaviour at prophase, their relative
size at metaphase, and their behaviour at meiosis.
The differentiation of the sex-chromosomes would be
followed by important genetic effects. Since mutations
within a chromosome can only be tested in different com-
binations when they can be freely distributed by crossing-
over, suppression of crossing-over prevents mutations
occurring in the Y from being so tested. Since crossing-
over does not occur, the Y cannot undergo any structural
change by means of interchange of parts. The Y-chromo-
some, therefore, during its evolution, would come to lose its
effectiveness in the matter of sex-determination, and its
place would be taken by the autosomes interacting with
theX.
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6o SEX-DETERMINATION
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GLOSSARY
ALLELOMORPH. Allelon, onc another; morpha, form. One of a pair
of alternative hereditary characters. The term is also applied
to those genes which can occupy one and the same locus upon
a particular chromosome.
ANAPHASE. Ana, up; phasis, appearance. The stage at which
daughter chromosomes move apart in nuclear division.
ATTACHMENT, (i) The spindlc attachment, q.v. (2) The permanent
fusion of two chromosomes (catination).
AUTOSOMES. Autos, sclf; soma, body. Those chromosomes in respect
of which both sexes are alike.
BALANCE, GENic. The Condition in which the genes are so related
and proportionally adjusted that in their action they yield
normal development of the organ.
BIVALENT (see Univalent). Bis, twice; valere, to be worth. A term
applied to double chromosomes formed by the coupling of
two chromosomes especially in the process of synapsis,
CENTROSOME. Kentroft, centre; soma, body. The self-propagating
body which, during mitosis in many organisms, lies at the two
poles of the spindle and appears to determine its orientation.
CHROMOSOMES. Chroma, colour; soma, body. Separate, deeply-
staining bodies commonly rod-shaped or loop-shaped into
which the substance of the nuclear network resolves itself
during mitosis and from which the nucleus is derived at the
end of mitosis.
CROSSING-OVER. The exchange of corresponding segments between
corresponding chromatids of different chromosomes.
DIPLOID. Diploos, double. The zygotic number of chromosomes
(an) as opposed to the gametic or haploid number (n).
DISJUNCTION. The separation of chromosomes at anaphase, par-
ticularly of the first meiotic division.
FIRST DIVISION. The first of two meiotic divisions; the heterotypic
or reduction division.
GAMETE. Gametes, spouse. Cells which are specialized for fertiliza-
tion and which normally cannot develop without it.
GENE. Gen, to produce or producing. The unit of Mendelian
heredity; a hypothetical elementary entity which determines
the development of a particular character. To the student of
heredity it is that which the atom is to the chemist.
GENOTYPE. Genus, a race; typus, an image, (i) The genetic constitu-
tion of an individual. (2) A class or group all the individuals
within which are identical in their genetic constitution.
GYNANDROMORPH. Gyne, woman; aner, man; morphe, form. An
individual exhibiting a combination of male and female
characters.
62
GLOSSARY 63
HAPLOiD. Haploos, single. Applied to the reduced or gametic
number of chromosomes.
HAPLO-DiPLOiD SYSTEM. That in which the sexes are distinguished
in that one is haploid, the other diploid.
HERMAPHRODITE. Hermaphroditos, combining both sexes. An
organism with both male and female reproductive organs.
HETEROGAMETic. Heteros, other; gametes, spouse. Elaborating
gametes of two kinds in respect of the elements of the sex-
determining mechanism.
HETEROKiNESis. Heteros, other; kinesis, change or movement.
That meiotic division in the course of which the sex-produc-
ing gametes become separated by differential distribution of
the sex-chromosomes.
HETEROPYCXOSis. Heteros, other; pyknos, dense. Precocious con-
densation of certain chromosomes in the prophase especially
of meiosis.
HETEROTYPIC DIVISION. The first meiotic division (falling into disuse).
HETEROZYGOTE. Heteros, other ; sygon, yolk. A Mendelian hybrid
in whose genetic constitution there are one or more recessive
genes and which, therefore, does not breed true. The off-
spring of a mating of parents which differed one from the
other in respect of one or more allelomorphic characters.
HOMEOTYPic DIVISION. The sccond division of meiosis (falling into
disuse).
HOMOGAMETIC. Homos, alike; gametes, spouse. Elaborating garnetes
all of a kind in respect of the elements of the sex-determining
mechanism.
HOMOZYGOTE. Homos, alike; zygon, a yolk. An individual in whose
genetic constitution each gene is present in the duplex state.
The offspring of a mating of two parents genetically identical
in respect of one or more Mendelian characters.
KARYOGAMY. Karyoti, nucleus; gametes, spouse. Fusion or nuclei at
the fertilization of an egg by a sperm.
KARYOKiNESis. Karyoti, nucleus; kinesis, change or movement
(=mitosis).
MATRICLINOUS. Mater, a mother. Inclining heredity toward the
maternal side.
MATURATION. The ripening or final stages in the formation of the
gametes by meiosis.
MEIOSIS. Meiosis, reduction. A form of mitosis in which the nucleus
divides twice and the chromosomes once.
MIDDLE PIECE. A term of vague meaning applied to the middle
region of the sperm.
MITOSIS. Mitos, a thread. The process by which the daughter
chromosomes are separated into two groups.
NON-DISJUNCTION. The failure of separation of paired chromo-
somes at meiosis and their passage to the same pole.
OOCYTE. Oon, an egg. The egg cell prior to the completion of the
maturation process.
64 SEX-DETERMINATION
OOGENESIS. Gametogenesis in the female.
PARTHENOGENESIS. Parthetios, a virgin. The development of an egg
without activation of a sperm.
PATRICULINOUS. Pater, a father. Inclining heredity toward the
paternal side.
PHENOTYPE. Phainein, to appear; typos, an image, (i) The sum of
the characters exhibited by an individual. (2) A group or class
composed of individuals all of whose characters are alike.
POLAR BODY. The expelled products of the two divisions of the
oocyte nucleus in animals.
POLYPLOID. Polys, many; aploos, one-fold; eidos, form. An organism
with more than two sets of homologous chromosomes.
REDUCTION. The halving of the chromosome number at meiosis.
SEGREGATION. The separation of chromosomes of paternal and
maternal origin at meiosis. Genetically, the separation during
the course of a breeding experiment of the alternative allelo-
morphic characters involved.
SEX-CHROMOSOMES. Chromosomcs in respect of which the sexes
differ.
SPERMATOCYTE. Sperma, a seed; hytos, a cell.
SPERM, SPERMATOZOON. The male gamete in animals.
SPERMATOGENESIS. Gametogenesis in the male.
SYNAPSIS. Synapto, to fuse together. Chromosome pairing at
zygotene.
TETRAD. Tetras, four, (i) A quartet of cells formed by meiosis in a
mother-cell. (2) The four chromatids making up a bivalent at
meiosis.
TRIPLOID. An organism having three sets of chromosomes.
UNIVALENT. A body at the first meiotic division corresponding with
a single chromosome.
x-CHROMOSOME. A sex-chromosome of which one sex possesses
one, the other two.
Y-CHROMOSOME. The sex-chromosome which is the mate of the
single X in the heterogametic sex.
ZYGOTE. Zygotes, yolked. (i) The cell formed by the union of the
gametes in the fertilized egg. (2) The individual derived
therefrom.
ZYGOTENE. Zygoti, yolk; taenia, a thread. The pairing threads and
the stage at which they occur in the prophase of meiosis.
AUTHOR INDEX
Aida, T., 47
Allen, C. E., 48
Asana, J. J., 15
Baltzer, F., 41
Bateson, W., and Punnett,
R. C, 6
Baur, E., 49
Bellamy, A. W., 47
Blakeslee, A. F., 48
Bostian, C. H., 31
Boveri, T., 13
Bridges, C. B., 21, 24, 27, 29, 42
Chavin, W., and Gordon, M.,
47
Correns, C, 5, 49
Crew, F. A. E., and Munro,
S. S., 45
Dobzhansky, T., and Bridges,
C. B, 43
and Schultz, J., 44
Doncaster, L., 5, 18, 29
Dordick, A., 31
Dreyfus, A., and Breuer, M. E.,
31
Du Bois, A. M., 33
Dzierzon, J., 30
Emerson, R. A., 50
Evans, H. M., and Swezy, O.,
4, 21
Federley, H., 44
Goldschmidt, R., 32, 33
Gross, J., II
Gulick, A., 13
Hartmann, M., 48
Henking, H., 10
Hughes-Schraeder, S., 13, 15,
16
Kihara, H., and Ono, T., 10
King, R. L., 15
and Beams, H. W., 16
Knapp, E., 49
Lebedeff, G. A., 42
McClung, C. E., 10
Mackay, E., and Allen, C. E.,
49
Matthey, R., 16
Mendel, G. J., 5
Metz, C. W., 32
and Schmuck, M. L., 33
and Smith, H. B., 33
Meurman, O., 49
Morgan, L. V., 26
Morgan, T. H., 23
and Bridges, C. B., 28, 29
and Sturtevant, A.
H., 29
Morrill, C. V., 13
Muller, H. J., 51
Mulsow, K., 13
Oguma, K., 15, 16
Ono, T., 10, 50
Paulmier, F. C, 10
Ray-Chauduri, S. P.,
Manna, G. K., 10
and
Santos, J. K., 49
Schrader, F., 27, 42
and Sturtevant, A. H., 32
Seller, J., 15, 45
Sharman, G. B., Mcintosh,
A. J., and Barber, H. N.^
10
Shull, G. H., 49
Sinetv", R. de, 10
Sneli; G. D., 31
65
66 SEX-DETERMINATION
Sokolovv, H. N., Tiniakow, Torvik-Greb, M., 30
G. C, and Trofimov, J. E.,
IS
Sonneborn, T. M., 48 Weismann, A.. 4
Standfuss, M., 44 White, M. J. D., 15, 16,
Stern, C, 27 30
Stevens, N. M., 11 Whiting, P. W., 30, 31
Sturtevant, A. H., 27, 42 Wilson, E. B., 11, 12
Sutton, W. S., II Winge, O., 40, 46, 49
i
SUBJECT INDEX
Abraxas, 5, 18, 29
Algae, 48
Anasa tristis, 10
Ancyr acanthus cystidicola, 13
Angiosperms, 49
Aplocheilus, 46
Bee, 30
Beetles, 13, 14
Bonellia viridis, 41
Brachystola, 1 1
Bn-onia, 5, 49
Br\'ophytes, 48
Bugs, 13, 14
Chlamydomonas eugawetos, 48
Dioecious plants, 14
Diptera, 14
Dioscorea siniiata, 49
Drosophila ynelanogaster,
attached X's, 26
fertility genes, 27
genetic intersexuality, 42
gynandromorphism, 27, 29
non-disjunction, 21
Drosophila simulans, 42
Drosophila virilis, 42
Elodea gigantea, 49
Euplotes, 48
Euscyrtus, 10
Fish, 46
Fowl, 15, 19, 45
Fungi, 48
Guinea-fowl, 15
Habrobracon, 30
Haemophilia, 21, 22
Heterakis, 13
Hierodula, 15
67
Homo- and heterogamety, 12,
21
Iceryini, 31
Lebistes, 46
Lepidoptera, 15
Lygaeus furcicus, 1 1
Lymantria dispar, 2 3
Maize, 50
Mammals, 14
Man, 4, 21
Mantis, 15
Meiosis, 4
Melandrium, .49
Mitosis, 4
Mucor, 48
Myriapods, 13
Nematodes, 13
Orphania, 10
Orthopterans, 13
Paramecium, 48
Paratenodera, 15
Paratylotropidia, 16
Peafowl, 15
Phasmids, 13
Pheasant, 15
Platypoecilus, 46
Praying Mantis, 16
Protenor belfragi, 12
Pygaera, 45
Pyrrhocoris apterus, 10, 11
Rat kangaroo, 10
Rumex acetosa, 10, 50
Saturnia, 44
Sciara, 32
Sex-ratio, 12, 16
Solenobia triquetrella, 45
68 SEX-DETERMINATION
Sphaerocarpus, 48 Telenomus fariai, 31
Spiders, 13 Tenebrio, 11
Stagomantis, 15 Tenodera, 15
Syromastes, 11, 12 Turkey, 15
Talaeporia tubulosa, 15 Woodcock, 15
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